Beyond binding: Antibody effector functions in infectious diseases

Nature Reviews Immunology

Volumn 18, Issue 1, 2018, Pages 46-61

  Lu, Lenette L ^a,b   Suscovich, Todd J ^a   Fortune, Sarah M ^b   Alter, Galit ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; TOXIN; VIRULENCE FACTOR;

ADAPTIVE IMMUNITY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY EFFECTOR FUNCTION; ANTIBODY STRUCTURE; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ANTIGEN PRESENTATION; ANTIMICROBIAL ACTIVITY; BACTERIAL CLEARANCE; COMPLEMENT ACTIVATION; DISEASE ACTIVITY; DRUG DESIGN; DRUG TARGETING; FUNGUS; FUNGUS CLEARANCE; HOST RESISTANCE; HUMAN; IMMUNE SYSTEM; INFECTION; INFLAMMATION; INNATE IMMUNITY; MICROORGANISM; NONHUMAN; PARASITE CLEARANCE; PATHOGEN CLEARANCE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; VIRAL CLEARANCE;

EID: 85039066883     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri.2017.106     Document Type: Review

References (207)

1. Behring, E. & Kitasato, S. Über das zustandekommen der diphtherie-immunität und der tetanus-immunität bei thieren [German]. Dtsch. Med. Wochenschrift 49, 1113-1114 (1890).
2. Hey, A. History and practice: antibodies in infectious diseases. Microbiol. Spectr. 3, AID-0026-2014 (2015).
3. Ehrlich, P. On immunity with special reference to cell life. Proc. R. Soc. Lond. 66, 424-448 (1899).
4. Metchnikoff, E. Untersuchung ueber die intracellulare verdauung bei wirbellosen thieren [German]. Arb. Zool. Inst. Univ. Wien u. Zool. Stat. Triest 5, 141-168 (1884).
5. Jerne, N. K. The natural-selection theory of antibody formation. Proc. Natl Acad. Sci. USA 41, 849-857 (1955).
6. Kohler, G. & Milstein, C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256, 495-497 (1975).
7. Ecker, D. M., Jones, S. D. & Levine, H. L. The therapeutic monoclonal antibody market. mAbs 7, 9-14 (2015).
8. Pignotti, M. S. et al. Consensus conference on the appropriateness of palivizumab prophylaxis in respiratory syncytial virus disease. Pediatr. Pulmonol. 51, 1088-1096 (2016).
9. Migone, T. S. et al. Raxibacumab for the treatment of inhalational anthrax. N. Engl. J. Med. 361, 135-144 (2009).
10. Wilcox, M. H. et al. Bezlotoxumab for prevention of recurrent Clostridium difficile infection. N. Engl. J. Med. 376, 305-317 (2017).
11. Weiner, G. J. Building better monoclonal antibody-based therapeutics. Nat. Rev. Cancer 15, 361-370 (2015).
12. Halstead, S. B., Mahalingam, S., Marovich, M. A., Ubol, S. & Mosser, D. M. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect. Dis. 10, 712-722 (2010).
13. Casadevall, A., Dadachova, E. & Pirofski, L. A. Passive antibody therapy for infectious diseases. Nat. Rev. Microbiol. 2, 695-703 (2004).
14. Zeitlin, L. et al. Antibody therapeutics for Ebola virus disease. Curr. Opin. Virol. 17, 45-49 (2016).
15. Wine, Y., Horton, A. P., Ippolito, G. C. & Georgiou, G. Serology in the 21 st century: the molecular-level analysis of the serum antibody repertoire. Curr. Opin. Immunol. 35, 89-97 (2015).
16. Plotkin, S. A. Complex correlates of protection after vaccination. Clin. Infect. Dis. 56, 1458-1465 (2013).
17. Pulendran, B. & Ahmed, R. Immunological mechanisms of vaccination. Nat. Immunol. 12, 509-517 (2011).
18. Ockenhouse, C. F. et al. Ad35.CS.01-RTS, S/AS01 heterologous prime boost vaccine efficacy against sporozoite challenge in healthy malaria-naive adults. PLoS ONE 10, e0131571 (2015).
19. Corey, L. et al. Immune correlates of vaccine protection against HIV-1 acquisition. Sci. Transl Med. 7, 310rv7 (2015).
20. Haynes, B. F. et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366, 1275-1286 (2012).
21. Rerks-Ngarm, S. et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361, 2209-2220 (2009).
22. Li, Z., Woo, C. J., Iglesias-Ussel, M. D., Ronai, D. & Scharff, M. D. The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 18, 1-11 (2004).
23. Mesin, L., Ersching, J. & Victora, G. D. Germinal center B cell dynamics. Immunity 45, 471-482 (2016).
24. Onoue, K., Grossberg, A. L., Yagi, Y. & Pressman, D. Immunoglobulin M antibodies with ten combining sites. Science 162, 574-576 (1968).
25. Czajkowsky, D. M. & Shao, Z. The human IgM pentamer is a mushroom-shaped molecule with a flexural bias. Proc. Natl Acad. Sci. USA 106, 14960-14965 (2009).
26. Sun, Z. et al. Semi-extended solution structure of human myeloma immunoglobulin D determined by constrained X-ray scattering. J. Mol. Biol. 353, 155-173 (2005).
27. Arnold, J. N., Wormald, M. R., Sim, R. B., Rudd, P. M. & Dwek, R. A. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 25, 21-50 (2007).
28. Lutz, C. et al. IgD can largely substitute for loss of IgM function in B cells. Nature 393, 797-801 (1998).
29. Chen, K. et al. Immunoglobulin D enhances immune surveillance by activating antimicrobial, proinflammatory and B cell-stimulating programs in basophils. Nat. Immunol. 10, 889-898 (2009).
30. Choi, J. H. et al. IgD class switching is initiated by microbiota and limited to mucosa-associated lymphoid tissue in mice. Proc. Natl Acad. Sci. USA 114, E1196-E1204 (2017).
31. Jefferis, R. Isotype and glycoform selection for antibody therapeutics. Arch. Biochem. Biophys. 526, 159-166 (2012).
32. Macpherson, A. J., McCoy, K. D., Johansen, F. E. & Brandtzaeg, P. The immune geography of IgA induction and function. Mucosal Immunol. 1, 11-22 (2008).
33. Wan, T. et al. The crystal structure of IgE Fc reveals an asymmetrically bent conformation. Nat. Immunol. 3, 681-686 (2002).
34. Rispens, T. & Vidarsson, G. in Antibody Fc (eds Ackerman, M. & Nimmerjahn, F.) 159-177 (Academic Press, 2013).
35. Dall'Acqua, W. F., Cook, K. E., Damschroder, M. M., Woods, R. M. & Wu, H. Modulation of the effector functions of a human IgG1 through engineering of its hinge region. J. Immunol. 177, 1129-1138 (2006).
36. Redpath, S., Michaelsen, T. E., Sandlie, I. & Clark, M. R. The influence of the hinge region length in binding of human IgG to human Fcgamma receptors. Hum. Immunol. 59, 720-727 (1998).
37. Ryan, M. H. et al. Proteolysis of purified IgGs by human and bacterial enzymes in vitro and the detection of specific proteolytic fragments of endogenous IgG in rheumatoid synovial fluid. Mol. Immunol. 45, 1837-1846 (2008).
38. Brezski, R. J. et al. Tumor-associated and microbial proteases compromise host IgG effector functions by a single cleavage proximal to the hinge. Proc. Natl Acad. Sci. USA 106, 17864-17869 (2009).
39. Vincents, B., von Pawel-Rammingen, U., Bjorck, L. & Abrahamson, M. Enzymatic characterization of the streptococcal endopeptidase, IdeS, reveals that it is a cysteine protease with strict specificity for IgG cleavage due to exosite binding. Biochemistry 43, 15540-15549 (2004).
40. Roux, K. H., Strelets, L. & Michaelsen, T. E. Flexibility of human IgG subclasses. J. Immunol. 159, 3372-3382 (1997).
41. Stapleton, N. M. et al. Competition for FcRn-mediated transport gives rise to short half-life of human IgG3 and offers therapeutic potential. Nat. Commun. 2, 599 (2011).
42. Senior, B. W. & Woof, J. M. Effect of mutations in the human immunoglobulin A1 (IgA1) hinge on its susceptibility to cleavage by diverse bacterial IgA1 proteases. Infection Immun. 73, 1515-1522 (2005).
43. Reusch, D. & Tejada, M. L. Fc glycans of therapeutic antibodies as critical quality attributes. Glycobiology 25, 1325-1334 (2015).
44. Ferrara, C. et al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcγRIII and antibodies lacking core fucose. Proc. Natl Acad. Sci. USA 108, 12669-12674 (2011).
45. Shields, R. L. et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. J. Biol. Chem. 277, 26733-26740 (2002).
46. Bournazos, S. et al. Broadly neutralizing anti-HIV-1 antibodies require Fc effector functions for in vivo activity. Cell 158, 1243-1253 (2014).
47. Woof, J. M. & Burton, D. R. Human antibody-Fc receptor interactions illuminated by crystal structures. Nat. Rev. Immunol. 4, 89-99 (2004).
48. Igietseme, J. U., Zhu, X. & Black, C. M. in Antibody Fc (eds Ackerman, M. & Nimmerjahn, F.) 269-281 (Academic Press, 2013).
49. Pincetic, A. et al. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat. Immunol. 15, 707-716 (2014).
50. Bruhns, P. et al. Specificity and affinity of human Fcγ receptors and their polymorphic variants for human IgG subclasses. Blood 113, 3716-3725 (2009).
51. Bruhns, P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119, 5640-5649 (2012).
52. Ravetch, J. V. in Fundamental Immunology Ch. 22, (ed. Paul, W. E.) (Lippincott Williams & Wilkins, 2003).
53. Jonsson, F. & Daeron, M. Mast cells and company. Front. Immunol. 3, 16 (2012).
54. Garred, P., Larsen, F., Seyfarth, J., Fujita, R. & Madsen, H. O. Mannose-binding lectin and its genetic variants. Genes Immun. 7, 85-94 (2006).
55. Ehrenstein, M. R. & Notley, C. A. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10, 778-786 (2010).
56. McEwan, W. A. et al. Intracellular antibody-bound pathogens stimulate immune signaling via the Fc receptor TRIM21. Nat. Immunol. 14, 327-336 (2013).
57. Roopenian, D. C. & Akilesh, S. FcRn: the neonatal Fc receptor comes of age. Nat. Rev. Immunol. 7, 715-725 (2007).
58. Johansen, F. E. & Kaetzel, C. S. Regulation of the polymeric immunoglobulin receptor and IgA transport: new advances in environmental factors that stimulate pIgR expression and its role in mucosal immunity. Mucosal Immunol. 4, 598-602 (2011).
59. Parren, P. W. et al. On the interaction of IgG subclasses with the low affinity FcγRIIa (CD32) on human monocytes, neutrophils, and platelets. Analysis of a functional polymorphism to human IgG2. J. Clin. Invest. 90, 1537-1546 (1992).
60. Cheung, N. K. et al. FCGR2A polymorphism is correlated with clinical outcome after immunotherapy of neuroblastoma with anti-GD2 antibody and granulocyte macrophage colony-stimulating factor. J. Clin. Oncol. 24, 2885-2890 (2006).
61. Zhang, W. et al. FCGR2A and FCGR3A polymorphisms associated with clinical outcome of epidermal growth factor receptor expressing metastatic colorectal cancer patients treated with single-agent cetuximab. J. Clin. Oncol. 25, 3712-3718 (2007).
62. Sinha, S. et al. Polymorphisms of TNF-enhancer and gene for FcγRIIa correlate with the severity of falciparum malaria in the ethnically diverse Indian population. Malar. J. 7, 13 (2008).
63. Esposito, S. et al. Role of polymorphisms of toll-like receptor (TLR) 4, TLR9, toll-interleukin 1 receptor domain containing adaptor protein (TIRAP) and FCGR2A genes in malaria susceptibility and severity in Burundian children. Malar J. 11, 196 (2012).
64. Forthal, D. N. et al. FcγRIIa genotype predicts progression of HIV infection. J. Immunol. 179, 7916-7923 (2007).
65. Yende, S. & Wunderink, R. Conflicting roles of FcγRIIa H131R polymorphism in pneumonia. Crit. Care Med. 39, 1577-1579 (2011).
66. Sole-Violan, J. et al. The Fcγ receptor IIA-H/H131 genotype is associated with bacteremia in pneumococcal community-acquired pneumonia. Crit. Care Med. 39, 1388-1393 (2011).
67. Garcia, G. et al. Asymptomatic dengue infection in a Cuban population confirms the protective role of the RR variant of the FcγRIIa polymorphism. Am. J. Trop. Med. Hyg. 82, 1153-1156 (2010).
68. Wu, J. et al. A novel polymorphism of FcγRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J. Clin. Invest. 100, 1059-1070 (1997).
69. Rekand, T., Langeland, N., Aarli, J. A. & Vedeler, C. A. Fcγ receptor IIIA polymorphism as a risk factor for acute poliomyelitis. J. Infect. Dis. 186, 1840-1843 (2002).
70. Forthal, D. N., Gabriel, E. E., Wang, A., Landucci, G. & Phan, T. B. Association of Fcγ receptor IIIa genotype with the rate of HIV infection after gp120 vaccination. Blood 120, 2836-2842 (2012).
71. Poonia, B., Kijak, G. H. & Pauza, C. D. High affinity allele for the gene of FCGR3A is risk factor for HIV infection and progression. PLoS ONE 5, e15562 (2010).
72. Daeron, M. Fc receptors as adaptive immunoreceptors. Curr. Top. Microbiol. Immunol. 382, 131-164 (2014).
73. Metzger, H. Transmembrane signaling: the joy of aggregation. J. Immunol. 149, 1477-1487 (1992).
74. Mitchell, A. J., Edwards, M. R. & Collins, A. M. Valency or wahlency: is the epitope diversity of the B-cell response regulated or chemically determined? Immunol. Cell Biol. 79, 507-511 (2001).
75. Nimmerjahn, F. & Ravetch, J. V. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 310, 1510-1512 (2005).
76. Abboud, N. et al. A requirement for FcγR in antibody-mediated bacterial toxin neutralization. J. Exp. Med. 207, 2395-2405 (2010).
77. DiLillo, D. J., Tan, G. S., Palese, P. & Ravetch, J. V. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat. Med. 20, 143-151 (2014).
78. Yuan, R., Clynes, R., Oh, J., Ravetch, J. V. & Scharff, M. D. Antibody-mediated modulation of Cryptococcus neoformans infection is dependent on distinct Fc receptor functions and IgG subclasses. J. Exp. Med. 187, 641-648 (1998).
79. Lux, A., Yu, X., Scanlan, C. N. & Nimmerjahn, F. Impact of immune complex size and glycosylation on IgG binding to human FcγRs. J. Immunol. 190, 4315-4323 (2013).
80. Pierson, T. C. et al. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1, 135-145 (2007).
81. Taborda, C. P., Rivera, J., Zaragoza, O. & Casadevall, A. More is not necessarily better: prozone-like effects in passive immunization with IgG. J. Immunol. 170, 3621-3630 (2003).
82. Kammanadiminti, S. et al. Combination therapy with antibiotics and anthrax immune globulin intravenous (AIGIV) is potentially more effective than antibiotics alone in rabbit model of inhalational anthrax. PLoS ONE 9, e106393 (2014).
83. Maynard, J. A. et al. Protection against anthrax toxin by recombinant antibody fragments correlates with antigen affinity. Nat. Biotechnol. 20, 597-601 (2002).
84. Little, S. F., Leppla, S. H. & Cora, E. Production and characterization of monoclonal antibodies to the protective antigen component of Bacillus anthracis toxin. Infection Immun. 56, 1807-1813 (1988).
85. Mabry, R. et al. Passive protection against anthrax by using a high-affinity antitoxin antibody fragment lacking an Fc region. Infection Immun. 73, 8362-8368 (2005).
86. Harvill, E. T. et al. Anamnestic protective immunity to Bacillus anthracis is antibody mediated but independent of complement and Fc receptors. Infection Immun. 76, 2177-2182 (2008).
87. Verma, A. et al. Analysis of the Fc gamma receptor-dependent component of neutralization measured by anthrax toxin neutralization assays. Clin. Vaccine Immunol.: CVI 16, 1405-1412 (2009).
88. Bournazos, S., Chow, S. K., Abboud, N., Casadevall, A. & Ravetch, J. V. Human IgG Fc domain engineering enhances antitoxin neutralizing antibody activity. J. Clin. Invest. 124, 725-729 (2014).
89. He, X. et al. Antibody-enhanced, Fc gamma receptor-mediated endocytosis of Clostridium difficile toxin A. Infection Immun. 77, 2294-2303 (2009).
90. 2 fragments and isotype variants of a recombinant human monoclonal antibody against Shiga toxin 2. Infection Immun. 78, 1376-1382 (2010).
91. Richman, D. D., Wrin, T., Little, S. J. & Petropoulos, C. J. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl Acad. Sci. USA 100, 4144-4149 (2003).
92. Walker, L. M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
93. Gautam, R. et al. A single injection of anti-HIV-1 antibodies protects against repeated SHIV challenges. Nature 533, 105-109 (2016).
94. Moldt, B. et al. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc. Natl Acad. Sci. USA 109, 18921-18925 (2012).
95. Law, M. et al. Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat. Med. 14, 25-27 (2008).
96. Kong, L. et al. Hepatitis C virus E2 envelope glycoprotein core structure. Science 342, 1090-1094 (2013).
97. Zhao, H. et al. Structural basis of Zika virus-specific antibody protection. Cell 166, 1016-1027 (2016).
98. Nybakken, G. E. et al. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437, 764-769 (2005).
99. Cockburn, J. J. et al. Structural insights into the neutralization mechanism of a higher primate antibody against dengue virus. EMBO J. 31, 767-779 (2012).
100. Irani, V. et al. Acquisition of functional antibodies that block the binding of erythrocyte-binding antigen 175 and protection against Plasmodium falciparum malaria in children. Clin. Infect. Dis. 1, 1244-1252 (2015).
101. Dutta, S., Haynes, J. D., Moch, J. K., Barbosa, A. & Lanar, D. E. Invasion-inhibitory antibodies inhibit proteolytic processing of apical membrane antigen 1 of Plasmodium falciparum merozoites. Proc. Natl Acad. Sci. USA 100, 12295-12300 (2003).
102. Varghese, R., Mikyas, Y., Stewart, P. L. & Ralston, R. Postentry neutralization of adenovirus type 5 by an antihexon antibody. J. Virol. 78, 12320-12332 (2004).
103. Ishii, Y. et al. Inhibition of nuclear entry of HPV16 pseudovirus-packaged DNA by an anti-HPV16 L2 neutralizing antibody. Virology 406, 181-188 (2010).
104. Aiyegbo, M. S. et al. Human rotavirus VP6-specific antibodies mediate intracellular neutralization by binding to a quaternary structure in the transcriptional pore. PLoS ONE 8, e61101 (2013).
105. Zhou, D. et al. Matrix protein-specific IgA antibody inhibits measles virus replication by intracellular neutralization. J. Virol. 85, 11090-11097 (2011).
106. Edelson, B. T. & Unanue, E. R. Intracellular antibody neutralizes Listeria growth. Immunity 14, 503-512 (2001).
107. Wang, X., Kikuchi, T. & Rikihisa, Y. Tw o monoclonal antibodies with defined epitopes of P44 major surface proteins neutralize Anaplasma phagocytophilum by distinct mechanisms. Infection Immun. 74, 1873-1882 (2006).
108. Hessell, A. J. et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature 449, 101-104 (2007).
109. Mullarkey, C. E. et al. Broadly neutralizing hemagglutinin stalk-specific antibodies induce potent phagocytosis of immune complexes by neutrophils in an Fc-dependent manner. mBio 7, e01624-16 (2016).
110. Kaur, R., Surendran, N., Ochs, M. & Pichichero, M. E. Human antibodies to PhtD, PcpA, and Ply reduce adherence to human lung epithelial cells and murine nasopharyngeal colonization by Streptococcus pneumoniae. Infection Immun. 82, 5069-5075 (2014).
111. Lam, H., Kesselly, A., Stegalkina, S., Kleanthous, H. & Yethon, J. A. Antibodies to PhnD inhibit staphylococcal biofilms. Infection Immun. 82, 3764-3774 (2014).
112. Gunn, B. M. et al. Enhanced binding of antibodies generated during chronic HIV infection to mucus component MUC16. Mucosal Immunol. 9, 1549-1558 (2016).
113. Wang, Y. Y. et al. IgG in cervicovaginal mucus traps HSV and prevents vaginal herpes infections. Mucosal Immunol. 7, 1036-1044 (2014).
114. Yauch, L. E., Lam, J. S. & Levitz, S. M. Direct inhibition of T-cell responses by the Cryptococcus capsular polysaccharide glucuronoxylomannan. PLoS Pathog. 2, e120 (2006).
115. Rodrigues, M. L. et al. Human antibodies against a purified glucosylceramide from Cryptococcus neoformans inhibit cell budding and fungal growth. Infection Immun. 68, 7049-7060 (2000).
116. McLean, G. R., Torres, M., Elguezabal, N., Nakouzi, A. & Casadevall, A. Isotype can affect the fine specificity of an antibody for a polysaccharide antigen. J. Immunol. 169, 1379-1386 (2002).
117. Diebolder, C. A. et al. Complement is activated by IgG hexamers assembled at the cell surface. Science 343, 1260-1263 (2014).
118. Merle, N. S., Noe, R., Halbwachs-Mecarelli, L., Fremeaux-Bacchi, V. & Roumenina, L. T. Complement system part II: role in immunity. Front. Immunol. 6, 257 (2015).
119. Merle, N. S., Church, S. E., Fremeaux-Bacchi, V. & Roumenina, L. T. Complement system part I: molecular mechanisms of activation and regulation. Front. Immunol. 6, 262 (2015).
120. Ram, S., Lewis, L. A. & Rice, P. A. Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin. Microbiol. Rev. 23, 740-780 (2010).
121. Benamu, E. & Montoya, J. G. Infections associated with the use of eculizumab: recommendations for prevention and prophylaxis. Curr. Opin. Infect. Dis. 29, 319-329 (2016).
122. Borrow, R. et al. Neisseria meningitidis group B correlates of protection and assay standardization-international meeting report Emory University, Atlanta, Georgia, United States, 16-17 March 2005. Vaccine 24, 5093-5107 (2006).
123. Goldschneider, I., Gotschlich, E. C. & Artenstein, M. S. Human immunity to the meningococcus. I. The role of humoral antibodies. J. Exp. Med. 129, 1307-1326 (1969).
124. Goldschneider, I., Gotschlich, E. C. & Artenstein, M. S. Human immunity to the meningococcus. II. Development of natural immunity. J. Exp. Med. 129, 1327-1348 (1969).
125. Wu, Y. et al. A potent broad-spectrum protective human monoclonal antibody crosslinking two haemagglutinin monomers of influenza A virus. Nat. Commun. 6, 7708 (2015).
126. Vogt, M. R. et al. Poorly neutralizing cross-reactive antibodies against the fusion loop of West Nile virus envelope protein protect in vivo via Fcγ receptor and complement-dependent effector mechanisms. J. Virol. 85, 11567-11580 (2011).
127. Benhnia, M. R. et al. Heavily isotype-dependent protective activities of human antibodies against vaccinia virus extracellular virion antigen B5. J. Virol. 83, 12355-12367 (2009).
128. Boyle, M. J. et al. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42, 580-590 (2015).
129. Zaragoza, O. & Casadevall, A. Monoclonal antibodies can affect complement deposition on the capsule of the pathogenic fungus Cryptococcus neoformans by both classical pathway activation and steric hindrance. Cell. Microbiol. 8, 1862-1876 (2006).
130. Taborda, C. P. & Casadevall, A. CR3 (CD11b/CD18) and CR4 (CD11c/CD18) are involved in complement-independent antibody-mediated phagocytosis of Cryptococcus neoformans. Immunity 16, 791-802 (2002).
131. Gonzalez, S. F. et al. Complement-dependent transport of antigen into B cell follicles. J. Immunol. 185, 2659-2664 (2010).
132. McCloskey, M. L., Curotto de Lafaille, M. A., Carroll, M. C. & Erlebacher, A. Acquisition and presentation of follicular dendritic cell-bound antigen by lymph node-resident dendritic cells. J. Exp. Med. 208, 135-148 (2011).
133. Phan, T. G., Grigorova, I., Okada, T. & Cyster, J. G. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 8, 992-1000 (2007).
134. Croix, D. A. et al. Antibody response to a T-dependent antigen requires B cell expression of complement receptors. J. Exp. Med. 183, 1857-1864 (1996).
135. Zeitlin, L. et al. Enhanced potency of a fucose-free monoclonal antibody being developed as an Ebola virus immunoprotectant. Proc. Natl Acad. Sci. USA 108, 20690-20694 (2011).
136. Umana, P., Jean-Mairet, J., Moudry, R., Amstutz, H. & Bailey, J. E. Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat. Biotechnol. 17, 176-180 (1999).
137. Weiskopf, K. & Weissman, I. L. Macrophages are critical effectors of antibody therapies for cancer. mAbs 7, 303-310 (2015).
138. Biburger, M., Lux, A. & Nimmerjahn, F. How immunoglobulin G antibodies kill target cells: revisiting an old paradigm. Adv. Immunol. 124, 67-94 (2014).
139. Bournazos, S., Wang, T. T. & Ravetch, J. V. The role and function of Fcγ receptors on myeloid cells. Microbiol. Spectr. 4, http://dx.doi.org/10.1128/microbiolspec.MCHD-0045-2016 (2016).
140. Peipp, M. et al. Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells. Blood 112, 2390-2399 (2008).
141. Nimmerjahn, F. & Ravetch, J. V. Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47 (2008).
142. Ackerman, M. E. et al. Polyfunctional HIV-specific antibody responses are associated with spontaneous HIV control. PLoS Pathog. 12, e1005315 (2016).
143. Barouch, D. H. et al. Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys. Cell 155, 531-539 (2013).
144. Chung, A. W. et al. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci. Transl Med. 6, 228ra38 (2014).
145. He, W. et al. Epitope specificity plays a critical role in regulating antibody-dependent cell-mediated cytotoxicity against influenza A virus. Proc. Natl Acad. Sci. USA 113, 11931-11936 (2016).
146. Tiendrebeogo, R. W. et al. Antibody-dependent cellular inhibition is associated with reduced risk against febrile malaria in a longitudinal cohort study involving Ghanaian children. Open Forum Infect. Dis. 2, ofv044 (2015).
147. Jafarshad, A. et al. A novel antibody-dependent cellular cytotoxicity mechanism involved in defense against malaria requires costimulation of monocytes FcγRII and FcγRIII. J. Immunol. 178, 3099-3106 (2007).
148. Moore, T. et al. Fc receptor regulation of protective immunity against Chlamydia trachomatis. Immunology 105, 213-221 (2002).
149. Lu, L. L. et al. A functional role for antibodies in tuberculosis. Cell 167, 433-443.e414 (2016).
150. Gounni, A. S. et al. High-affinity IgE receptor on eosinophils is involved in defence against parasites. Nature 367, 183-186 (1994).
151. Joseph, M., Auriault, C., Capron, A., Vorng, H. & Viens, P. A new function for platelets: IgE-dependent killing of schistosomes. Nature 303, 810-812 (1983).
152. Bruel, T. et al. Elimination of HIV-1-infected cells by broadly neutralizing antibodies. Nat. Commun. 7, 10844 (2016).
153. Lee, W. S., Parsons, M. S., Kent, S. J. & Lichtfuss, M. Can HIV-1-specific ADCC assist the clearance of reactivated latently infected cells? Front. Immunol. 6, 265 (2015).
154. Lee, W. S. et al. Antibody-dependent cellular cytotoxicity against reactivated HIV-1-infected cells. J. Virol. 90, 2021-2030 (2015).
155. Scheid, J. F. et al. HIV-1 antibody 3BNC117 suppresses viral rebound in humans during treatment interruption. Nature 535, 556-560 (2016).
156. Caskey, M. et al. Antibody 10-1074 suppresses viremia in HIV-1-infected individuals. Nat. Med. 23, 185-191 (2017).
157. Lu, C. L. et al. Enhanced clearance of HIV-1-infected cells by broadly neutralizing antibodies against HIV-1 in vivo. Science 352, 1001-1004 (2016).
158. Lynch, R. M. et al. Virologic effects of broadly neutralizing antibody VRC01 administration during chronic HIV-1 infection. Sci. Transl Med. 7, 319ra206 (2015).
159. Barouch, D. H. et al. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys. Nature 503, 224-228 (2013).
160. Shingai, M. et al. Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503, 277-280 (2013).
161. Bolton, D. L. et al. Human immunodeficiency virus type 1 monoclonal antibodies suppress acute simian-human immunodeficiency virus viremia and limit seeding of cell-associated viral reservoirs. J. Virol. 90, 1321-1332 (2015).
162. Weber, S. S. & Oxenius, A. in Antibody Fc (eds Ackerman, M. & Nimmerjahn, F.) 29-47 (Academic Press, 2013).
163. Boross, P. et al. FcRγ-chain ITAM signaling is critically required for cross-presentation of soluble antibody-antigen complexes by dendritic cells. J. Immunol. 193, 5506-5514 (2014).
164. Bergtold, A., Desai, D. D., Gavhane, A. & Clynes, R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23, 503-514 (2005).
165. Rittirsch, D. et al. Cross-talk between TLR4 and FcγReceptorIII (CD16) pathways. PLoS Pathog. 5, e1000464 (2009).
166. Anthony, R. M., Wermeling, F., Karlsson, M. C. & Ravetch, J. V. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc. Natl Acad. Sci. USA 105, 19571-19578 (2008).
167. van Egmond, M., Vidarsson, G. & Bakema, J. E. Crosstalk between pathogen recognizing Toll-like receptors and immunoglobulin Fc receptors in immunity. Immunol. Rev. 268, 311-327 (2015).
168. Hoving, J. C., Wilson, G. J. & Brown, G. D. Signalling C-type lectin receptors, microbial recognition and immunity. Cell. Microbiol. 16, 185-194 (2014).
169. Joller, N. et al. Antibodies protect against intracellular bacteria by Fc receptor-mediated lysosomal targeting. Proc. Natl Acad. Sci. USA 107, 20441-20446 (2010).
170. Herrada, A. A., Contreras, F. J., Tobar, J. A., Pacheco, R. & Kalergis, A. M. Immune complex-induced enhancement of bacterial antigen presentation requires Fcγ receptor III expression on dendritic cells. Proc. Natl Acad. Sci. USA 104, 13402-13407 (2007).
171. Guilliams, M., Bruhns, P., Saeys, Y., Hammad, H. & Lambrecht, B. N. The function of Fcγ receptors in dendritic cells and macrophages. Nat. Rev. Immunol. 14, 94-108 (2014).
172. van Kessel, K. P., Bestebroer, J. & van Strijp, J. A. Neutrophil-mediated phagocytosis of Staphylococcus aureus. Front. Immunol. 5, 467 (2014).
173. Sylvestre, D. L. & Ravetch, J. V. Fc receptors initiate the Arthus reaction: redefining the inflammatory cascade. Science 265, 1095-1098 (1994).
174. Hawkes, R. A. Enhancement of the Infectivity of arboviruses by specific antisera produced in domestic fowls. Aust. J. Exp. Biol. Med. Sci. 42, 465-482 (1964).
175. Ayala-Nunez, N. V. et al. How antibodies alter the cell entry pathway of dengue virus particles in macrophages. Sci. Rep. 6, 28768 (2016).
176. Goncalvez, A. P., Engle, R. E., St Claire, M., Purcell, R. H. & Lai, C. J. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc. Natl Acad. Sci. USA 104, 9422-9427 (2007).
177. Beltramello, M. et al. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8, 271-283 (2010).
178. Dejnirattisai, W. et al. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with Zika virus. Nat. Immunol. 17, 1102-1108 (2016).
179. Polack, F. P. et al. A role for immune complexes in enhanced respiratory syncytial virus disease. J. Exp. Med. 196, 859-865 (2002).
180. Ponnuraj, E. M., Springer, J., Hayward, A. R., Wilson, H. & Simoes, E. A. Antibody-dependent enhancement, a possible mechanism in augmented pulmonary disease of respiratory syncytial virus in the Bonnet monkey model. J. Infecti. Diseases 187, 1257-1263 (2003).
181. Kane, M. M. & Mosser, D. M. The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 166, 1141-1147 (2001).
182. Buxbaum, L. U. & Scott, P. Interleukin 10-and Fcγ receptor-deficient mice resolve Leishmania mexicana lesions. Infection Immun. 73, 2101-2108 (2005).
183. Sutterwala, F. S., Noel, G. J., Salgame, P. & Mosser, D. M. Reversal of proinflammatory responses by ligating the macrophage Fcγ receptor type I. J. Exp. Med. 188, 217-222 (1998).
184. Nowakowski, A. et al. Potent neutralization of botulinum neurotoxin by recombinant oligoclonal antibody. Proc. Natl Acad. Sci. USA 99, 11346-11350 (2002).
185. Qiu, X. et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 514, 47-53 (2014).
186. Lyon, G. M. et al. Clinical care of two patients with Ebola virus disease in the United States. N. Engl. J. Med. 371, 2402-2409 (2014).
187. Howell, K. A. et al. Cooperativity enables non-neutralizing antibodies to neutralize Ebolavirus. Cell Rep. 19, 413-424 (2017).
188. Chung, A. W. et al. Dissecting polyclonal vaccine-induced humoral immunity against HIV using systems serology. Cell 163, 988-998 (2015).
189. Nakaya, H. I. et al. Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 12, 786-795 (2011).
190. Kazmin, D. et al. Systems analysis of protective immune responses to RTS, S malaria vaccination in humans. Proc. Natl Acad. Sci. USA 114, 2425-2430 (2017).
191. Kasturi, S. P. et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 470, 543-547 (2011).
192. Horton, R. E. & Vidarsson, G. Antibodies and their receptors: different potential roles in mucosal defense. Front. Immunol. 4, 200 (2013).
193. Engelhardt, B., Vajkoczy, P. & Weller, R. O. The movers and shapers in immune privilege of the CNS. Nat. Immunol. 18, 123-131 (2017).
194. DiLillo, D. J. & Ravetch, J. V. Differential Fc-receptor engagement drives an anti-tumor vaccinal effect. Cell 161, 1035-1045 (2015).
195. Abes, R., Gelize, E., Fridman, W. H. & Teillaud, J. L. Long-lasting antitumor protection by anti-CD20 antibody through cellular immune response. Blood 116, 926-934 (2010).
196. Stavenhagen, K., Plomp, R. & Wuhrer, M. Site-specific protein N-and O-glycosylation analysis by a C18-porous graphitized carbon-liquid chromatography-electrospray ionization mass spectrometry approach using pronase treated glycopeptides. Anal. Chem. 87, 11691-11699 (2015).
197. Plomp, R. et al. Hinge-region O-glycosylation of human immunoglobulin G3 (IgG3). Mol. Cell. Proteom. 14, 1373-1384 (2015).
198. Boehm, M. K., Woof, J. M., Kerr, M. A. & Perkins, S. J. The Fab and Fc fragments of IgA1 exhibit a different arrangement from that in IgG: a study by X-ray and neutron solution scattering and homology modelling. J. Mol. Biol. 286, 1421-1447 (1999).
199. Kubo, S., Nakayama, T., Matsuoka, K., Yonekawa, H. & Karasuyama, H. Long term maintenance of IgE-mediated memory in mast cells in the absence of detectable serum IgE. J. Immunol. 170, 775-780 (2003).
200. Shade, K. T. et al. A single glycan on IgE is indispensable for initiation of anaphylaxis. J. Exp. Med. 212, 457-467 (2015).
201. Karsten, C. M. et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcγRIIB and dectin-1. Nat. Med. 18, 1401-1406 (2012).
202. Sondermann, P., Pincetic, A., Maamary, J., Lammens, K. & Ravetch, J. V. General mechanism for modulating immunoglobulin effector function. Proc. Natl Acad. Sci. USA 110, 9868-9872 (2013).
203. H 2 pathway. Nature 475, 110-113 (2011).
204. Gala, F. A. & Morrison, S. L. The role of constant region carbohydrate in the assembly and secretion of human IgD and IgA1. J. Biol. Chem. 277, 29005-29011 (2002).
205. Phalipon, A. et al. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity 17, 107-115 (2002).
206. Basset, C. et al. Glycosylation of immunoglobulin A influences its receptor binding. Scand. J. Immunol. 50, 572-579 (1999).
207. Saji, F., Samejima Y., Kamiura S., & Koyama M. Dynamics of immunoglobulins at the feto-maternal interface. Rev. Reprod. 4, 81-89 (1999).